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Current HIV Research

Author(s): Dmitry Neshumaev*, Aleksey Lebedev, Marina Malysheva, Anatoly Boyko, Sergey Skudarnov, Ekaterina Ozhmegova, Anastasia Antonova, Elena Kazennova and Marina Bobkova

DOI: 10.2174/1570162X17666190618155816

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Molecular Surveillance of HIV-1 Infection in Krasnoyarsk Region, Russia: Epidemiology, Phylodynamics and Phylogeography

Page: [114 - 125] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Background: The information about the dynamics of the viral population and migration events that affect the epidemic in different parts of the Russia is insufficient. Possibly, the huge size of the country and limited transport accessibility to certain territories may determine unique traits of the HIV-1 evolutionary history in different regions.

Objective: The aim of this study was to explore the genetic diversity of HIV-1 in the Krasnoyarsk region and reconstruct spatial-temporal dynamics of the infection in the region.

Methods: The demographic and virologic data from 281 HIV-infected individuals in Krasnoyarsk region collected during 2011-2016 were analyzed. The time to the most recent common ancestor, evolutionary rates, population growth, and ancestral geographic movements was estimated using Bayesian coalescent-based methods.

Results: The study revealed moderate diversity of the HIV-1 subtypes found in the region, which included A6 (92.3%), CRF063_02A (4.3%), B (1.1%), and unique recombinants (2.5%). Phylogenetic reconstruction revealed that the A6 subtype was introduced into Krasnoyarsk region by one viral lineage, which arose around 1996.9 (1994.5-1999.5). The phylogeography analysis pointed to Krasnoyarsk city as the geographical center of the epidemic, which further spread to central neighboring districts of the region. At least two epidemic growth phases of subtype A6 were identified which included exponential growth in early-2000s followed by the decline in the mid/late 2010s.

Conclusion: This study demonstrates a change in the genetic diversity of HIV-1 in the Krasnoyarsk region. At the beginning of the epidemic, subtype A6 prevailed, subtypes B and CRF063_02A appeared in the region later.

Keywords: HIV-1, Russia, Krasnoyarsk region, phylodynamic, phylogeography, molecular epidemiology, Bayesian analysis, epidemiological monitoring.

Graphical Abstract

[1]
UNAIDS, Eastern Europe & Central Asia [cited 2019 Feb 10]. Available from:. http://www.unaids.org/en/regionscountries/easterneuropeandcentralasia
[2]
UNAIDS, Russian Federation [cited 2019 Feb 10]. Available from:. http://www.unaids.org/en/regionscountries/countries/russianfederation
[3]
HIV data in the Russian Federation, Federal AIDS center [cited 2019 Feb10] Available from:. http://helper-nov.ru/news.php?id=55
[4]
Foley BT, Leitner T, Paraskevis D, Peeters M. Primate immunodeficiency virus classification and nomenclature. Review Infect Genet Evol 2016; 46: 150-158 .
[http://dx.doi.org/[http://10.1016/j.meegid.2016.10.018] [PMID: 27789390]
[5]
Lapovok IA, Lopatukhin AE, Kireev DE, et al. Molecular epidemiological analysis of HIV-1 variants circulating in Russia in 1987-2015. Ter Arkh 2017; 89(11): 44-9.
[http://dx.doi.org/10.17116/terarkh2017891144-49] [PMID: 29260745]
[6]
Novitsky VA, Montano MA, Essex M. Molecular epidemiology of an HIV-1 subtype A subcluster among injection drug users in the Southern Ukraine. AIDS Res Hum Retroviruses 1998; 14(12): 1079-85.
[http://dx.doi.org/10.1089/aid.1998.14.1079] [PMID: 9718124]
[7]
Díez-Fuertes F, Cabello M, Thomson MM. Bayesian phylogeographic analyses clarify the origin of the HIV-1 subtype A variant circulating in former Soviet Union’s countries. Infect Genet Evol 2015; 33: 197-205.
[http://dx.doi.org/10.1016/j.meegid.2015.05.003] [PMID: 25952568]
[8]
Dehne KL, Khodakevich L, Hamers FF, Schwartländer B. The HIV/AIDS epidemic in eastern Europe: Recent patterns and trends and their implications for policy-making. AIDS 1999; 13(7): 741-9.
[http://dx.doi.org/10.1097/00002030-199905070-00002] [PMID: 10357372]
[9]
Hamers FF, Batter V, Downs AM, Alix J, Cazein F, Brunet JB. The HIV epidemic associated with injecting drug use in Europe: Geographic and time trends. AIDS 1997; 11(11): 1365-74.
[http://dx.doi.org/10.1097/00002030-199711000-00011] [PMID: 9302447]
[10]
Lukashov VV, Karamov EV, Eremin VF, Titov LP, Goudsmit J. Extreme founder effect in an HIV type 1 subtype A epidemic among drug users in Svetlogorsk, Belarus. AIDS Res Hum Retroviruses 1998; 14(14): 1299-303.
[http://dx.doi.org/10.1089/aid.1998.14.1299] [PMID: 9764916]
[11]
Bobkov A, Kazennova E, Khanina T, et al. An HIV type 1 subtype A strain of low genetic diversity continues to spread among injecting drug users in Russia: Study of the new local outbreaks in Moscow and Irkutsk. AIDS Res Hum Retroviruses 2001; 17(3): 257-61.
[http://dx.doi.org/10.1089/088922201750063188] [PMID: 11177409]
[12]
Pandrea I, Descamps D, Collin G, et al. HIV type 1 genetic diversity and genotypic drug susceptibility in the Republic of Moldova. AIDS Res Hum Retroviruses 2001; 17(13): 1297-304.
[http://dx.doi.org/10.1089/088922201750461375] [PMID: 11559431]
[13]
Kurbanov F, Kondo M, Tanaka Y, et al. Human immunodeficiency virus in Uzbekistan: Epidemiological and genetic analyses. AIDS Res Hum Retroviruses 2003; 19(9): 731-8.
[http://dx.doi.org/10.1089/088922203769232520] [PMID: 14585203]
[14]
Bobkov AF, Zverev SIa, Bobkova MR, et al. Epidemiological and genetical characteristics of first forty cases of HIV infection in Perm region. Vopr Virusol 2000; 45(4): 18-21.
[PMID: 10971960]
[15]
Bobkov AF, Kazennova EV, Selimova LM, et al. Temporal trends in the HIV-1 epidemic in Russia: Predominance of subtype A. J Med Virol 2004; 74(2): 191-6.
[http://dx.doi.org/10.1002/jmv.20177] [PMID: 15332265]
[16]
Rhodes T, Ball A, Stimson GV, et al. HIV infection associated with drug injecting in the newly independent states, eastern Europe: the social and economic context of epidemics. Addiction 1999; 94(9): 1323-36.
[http://dx.doi.org/10.1046/j.1360-0443.1999.94913235.x] [PMID: 10615718]
[17]
Barnett T, Whiteside A, Khodakevich L, Kruglov Y, Steshenko V. The HIV/AIDS epidemic in Ukraine: Its potential social and economic impact. Soc Sci Med 2000; 51(9): 1387-403.
[http://dx.doi.org/10.1016/S0277-9536(00)00104-0] [PMID: 11037225]
[18]
HIV data in the Russian Federation, Federal AIDS center [cited 2019 Feb10]. Available from:. http://www.hivrussia.ru/stat/2000.shtml
[19]
HIV data in the Russian Federation, Federal AIDS center [cited 2019 Feb10] Available from:. http://www.hivrussia.ru/files/bul_30/08.pdf
[20]
Burchell AN, Calzavara LM, Orekhovsky V, Ladnaya NN. Characterization of an emerging heterosexual HIV epidemic in Russia. Sex Transm Dis 2008; 35(9): 807-13.
[http://dx.doi.org/10.1097/OLQ.0b013e3181728a9e] [PMID: 18496470]
[21]
Bobkova M. Current status of HIV-1 diversity and drug resistance monitoring in the former USSR. AIDS Rev 2013; 15(4): 204-12.
[PMID: 24192601]
[22]
Kazennova EV, Vasil’ev AV, Lapovok IA, et al. [HIV-1 genetic variants in the Asian part of Russia: a study (2005-2010)]. Vopr Virusol 2013; 58(4): 28-35.
[PMID: 24354062]
[23]
Bogachev VV, Totmenin AV, Baryshev PB, Meshcheriakova IuV, Chernousova NIA, Gashnikova NM. Molecular-genetic characteristic of HIV-1 A and B subtypes variants isolated in Novosibirsk region. Zh Mikrobiol Epidemiol Immunobiol 2012; 6(6): 45-52.
[PMID: 23297631]
[24]
Baryshev PB, Bogachev VV, Gashnikova NM. Genetic characterization of an isolate of HIV type 1 AG recombinant form circulating in Siberia, Russia. Arch Virol 2012; 157(12): 2335-41.
[http://dx.doi.org/10.1007/s00705-012-1442-4] [PMID: 22903393]
[25]
Lebedev A, Lebedeva N, Moskaleychik F, Pronin A, Kazennova E, Bobkova M. Human immunodeficiency virus-1 diversity in the Moscow region, Russia: Phylodynamics of the most common subtypes. Front Microbiol 2019; 10: 320.
[http://dx.doi.org/10.3389/fmicb.2019.00320] [PMID: 30863382]
[26]
Sukhanova AL, Kazennova EV, Bobkova MR, et al. Variants of human immunodeficiency virus type 1, detected in Russia among those infected by the sexual route. Vopr Virusol 2004; 49(1): 4-7.
[PMID: 15017845]
[27]
Bobkov AF, Pokrovskiĭ VV, Selimova LM, et al. Genotyping and phylogenetic analysis of HIV-1 isolates circulating in Russia. Vopr Virusol 1997; 42(1): 13-6.
[PMID: 9103036]
[28]
Lukashov VV, Cornelissen MT, Goudsmit J, et al. Simultaneous introduction of distinct HIV-1 subtypes into different risk groups in Russia, Byelorussia and Lithuania. AIDS 1995; 9(5): 435-9.
[http://dx.doi.org/10.1097/00002030-199509050-00004] [PMID: 7639968]
[29]
Kazennova E, Laga V, Lapovok I, et al. HIV-1 genetic variants in the Russian Far East. AIDS Res Hum Retroviruses 2014; 30(8): 742-52.
[http://dx.doi.org/10.1089/aid.2013.0194] [PMID: 24773167]
[30]
Kazennova E, Laga V, Gromov K, et al. Genetic variants of HIV type 1 in men who have sex with men in Russia. AIDS Res Hum Retroviruses 2017; 33(10): 1061-4.
[http://dx.doi.org/10.1089/aid.2017.0078] [PMID: 28443684]
[31]
Shcherbakova NS, Shalamova LA, Delgado E, et al. Short communication: Molecular epidemiology, phylogeny, and phylodynamics of CRF63_02A1, a recently originated HIV-1 circulating recombinant form spreading in Siberia. AIDS Res Hum Retroviruses 2014; 30(9): 912-9.
[http://dx.doi.org/10.1089/aid.2014.0075] [PMID: 25050828]
[32]
Kostaki EG, Karamitros T, Bobkova M, et al. Spatiotemporal characteristics of the HIV-1 CRF02_AG/CRF63_02A1 epidemic in Russia and Central Asia. AIDS Res Hum Retroviruses 2018; 34(5): 415-20.
[http://dx.doi.org/10.1089/aid.2017.0233] [PMID: 29455562]
[33]
Gashnikova NM, Bogachev VV, Baryshev PB, et al. A rapid expansion of HIV-1 CRF63_02A1 among newly diagnosed HIV-infected individuals in the Tomsk Region, Russia. AIDS Res Hum Retroviruses 2015; 31(4): 456-60.
[http://dx.doi.org/10.1089/aid.2014.0375] [PMID: 25738513]
[34]
Gashnikova NM, Zyryanova DP, Astakhova EM, et al. Predominance of CRF63_02A1 and multiple patterns of unique recombinant forms of CRF63_A1 among individuals with newly diagnosed HIV-1 infection in Kemerovo Oblast, Russia. Arch Virol 2017; 162(2): 379-90.
[http://dx.doi.org/10.1007/s00705-016-3120-4] [PMID: 27761744]
[35]
Lemey P, Rambaut A, Drummond AJ, Suchard MA. Bayesian phylogeography finds its roots. PLOS Comput Biol 2009; 5(9)e1000520
[http://dx.doi.org/10.1371/journal.pcbi.1000520] [PMID: 19779555]
[36]
Trovão NS, Suchard MA, Baele G, Gilbert M, Lemey P. Bayesian inference reveals host-specific contributions to the epidemic expansion of influenza A H5N1. Mol Biol Evol 2015; 32(12): 3264-75.
[http://dx.doi.org/10.1093/molbev/msv185] [PMID: 26341298]
[37]
Rumyantseva OA, Olkhovskiy IA, Malysheva MA, et al. Epidemiological networks and drug resistance of HIV type 1 in Krasnoyarsk region, Russia. AIDS Res Hum Retroviruses 2009; 25(9): 931-6.
[http://dx.doi.org/10.1089/aid.2009.0075] [PMID: 19689192]
[38]
Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 2017. Epub ahead of print
[http://dx.doi.org/10.1093/bib/bbx108] [PMID: 28968734]
[39]
Struck D, Lawyer G, Ternes AM, Schmit JC, Bercoff DP. COMET: adaptive context-based modeling for ultrafast HIV-1 subtype identification. Nucleic Acids Res 2014; 42(18)e144
[http://dx.doi.org/10.1093/nar/gku739] [PMID: 25120265]
[40]
Pineda-Peña AC, Faria NR, Imbrechts S, et al. Automated subtyping of HIV-1 genetic sequences for clinical and surveillance purposes: performance evaluation of the new REGA version 3 and seven other tools. Infect Genet Evol 2013; 19: 337-48.
[http://dx.doi.org/10.1016/j.meegid.2013.04.032] [PMID: 23660484]
[41]
Schultz AK, Bulla I, Abdou-Chekaraou M, et al. jpHMM: recombination analysis in viruses with circular genomes such as the hepatitis B virus Nucleic Acids Res 40(Web Server issue)2012; : W193-8.
[42]
Johnson VA, Calvez V, Günthard HF, et al. 2011 update of the drug resistance mutations in HIV-1. Top Antivir Med 2011; 19(4): 156-64.
[PMID: 22156218]
[43]
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: More models, new heuristics and parallel computing. Nat Methods 2012; 9(8): 772.
[http://dx.doi.org/10.1038/nmeth.2109] [PMID: 22847109]
[44]
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32(1): 268-74.
[http://dx.doi.org/10.1093/molbev/msu300] [PMID: 25371430]
[45]
Shimodaira H, Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 1999; 16: 1114-6.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a026201]
[46]
Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 2018; 4(1)vey016
[http://dx.doi.org/10.1093/ve/vey016] [PMID: 29942656]
[47]
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 2018; 67(5): 901-4.
[http://dx.doi.org/10.1093/sysbio/syy032] [PMID: 29718447]
[48]
Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44(W1)W242-5
[http://dx.doi.org/10.1093/nar/gkw290] [PMID: 27095192]
[49]
Bielejec F, Rambaut A, Suchard MA, Lemey P. SPREAD: Spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics 2011; 27(20): 2910-2.
[http://dx.doi.org/10.1093/bioinformatics/btr481] [PMID: 21911333]
[50]
Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016; 2(1)vew007
[http://dx.doi.org/10.1093/ve/vew007] [PMID: 27774300]
[51]
Kazennova EV, Laga VY, Gromov KB, et al. Molecular epidemiological analysis of hiv infection in northern seaports of Russia. Vopr Virusol 2017; 62(4): 154-61.
[PMID: 29733164]
[52]
Delatorre E, Mir D, Bello G. Spatiotemporal dynamics of the HIV-1 subtype G epidemic in West and Central Africa. PLoS One 2014; 9(2)e98908
[http://dx.doi.org/10.1371/journal.pone.0098908] [PMID: 24918930]
[53]
Yebra G, Ragonnet-Cronin M, Ssemwanga D, et al. Analysis of the history and spread of HIV-1 in Uganda using phylodynamics. J Gen Virol 2015; 96(Pt 7): 1890-8.
[http://dx.doi.org/10.1099/vir.0.000107] [PMID: 25724670]
[54]
Gräf T, Machado Fritsch H, de Medeiros RM, Maletich Junqueira D, Esteves de Matos Almeida S, Pinto AR. Comprehensive characterization of HIV-1 molecular epidemiology and demographic history in the Brazilian region most heavily affected by AIDS. J Virol 2016; 90(18): 8160-8.
[http://dx.doi.org/10.1128/JVI.00363-16] [PMID: 27384663]
[55]
Wang X, He X, Zhong P, et al. Phylodynamics of major CRF01_AE epidemic clusters circulating in mainland of China. Sci Rep 2017; 7(1): 6330.
[http://dx.doi.org/10.1038/s41598-017-06573-6] [PMID: 28740095]
[56]
Smolskaya T, Liitsola K, Zetterberg V, et al. HIV epidemiology in the Northwestern Federal District of Russia: Dominance of HIV type 1 subtype A. AIDS Res Hum Retroviruses 2006; 22(11): 1074-80.
[http://dx.doi.org/10.1089/aid.2006.22.1074] [PMID: 17147492]
[57]
Kazennova EV, Antonova OV, Kuzin SN, et al. Molecular and epidemiology studies of HIV-1 prevalence in the Republic of Sakha (Yakutia). Vopr Virusol 2011; 56(5): 30-4.
[PMID: 22171475]
[58]
Lebedev AV, Kazennova EV, Zverev SY, et al. Analysis of the env gene variability of the IDU-A HIV-1 variant in the outbreak of the HIV infection epidemic in Perm region of Russia (1996-2011). Vopr Virusol 2016; 61(5): 222-9.
[PMID: 29323855]
[59]
Karamov E, Epremyan K, Siniavin A, et al. HIV-1 genetic diversity in recently diagnosed infections in Moscow: Predominance of Afsu, frequent branching in clusters, and circulation of the iberian subtype G variant. AIDS Res Hum Retroviruses 2018; 34(7): 629-34.
[http://dx.doi.org/10.1089/aid.2018.0055] [PMID: 29587492]
[60]
Kazennova EV, Lapovok IA, Lebedev AV, et al. Analysis of HIV drugs resistance in Privolzhskiy federal district of the Russian Federation. HIV Infect Immunosup Dis 2015; 7(3): 56-66.
[61]
Altman D, Aggleton P, Williams M, et al. Men who have sex with men: stigma and discrimination. Lancet 2012; 380(9839): 439-45.
[http://dx.doi.org/10.1016/S0140-6736(12)60920-9] [PMID: 22819652]
[62]
Thomson MM, Vinogradova A, Delgado E, et al. Molecular epidemiology of HIV-1 in St Petersburg, Russia: Predominance of subtype A, former Soviet Union variant, and identification of intrasubtype subclusters. J Acquir Immune Defic Syndr 2009; 51(3): 332-9.
[http://dx.doi.org/10.1097/QAI.0b013e31819c1757] [PMID: 19363451]
[63]
Dukhovlinova E, Masharsky A, Toussova O, et al. Two independent HIV epidemics in St. Petersburg, Russia revealed by molecular epidemiology. AIDS Res Hum Retroviruses 2015; 31(6): 608-14.
[http://dx.doi.org/10.1089/aid.2014.0150] [PMID: 25417740]
[64]
Chow WZ, Takebe Y, Syafina NE, et al. A newly emerging HIV-1 recombinant lineage (CRF58_01B) disseminating among people who inject drugs in Malaysia. PLoS One 2014; 9(1)e85250
[http://dx.doi.org/10.1371/journal.pone.0085250] [PMID: 24465513]
[65]
Liu W, Feng Y, Wang C, et al. Identification of a novel HIV type 1 CRF01_AE/CRF07_BC recombinant virus in men who have sex with men in GuangXi, China. AIDS Res Hum Retroviruses 2019; 35(4): 402-6.
[http://dx.doi.org/10.1089/aid.2018.0157] [PMID: 30152708]
[66]
Li X, Zang X, Ning C, et al. Molecular epidemiology of HIV-1 in Jilin province, northeastern China: emergence of a new CRF07_BC transmission cluster and intersubtype recombinants. PLoS One 2014; 9(10)e110738
[http://dx.doi.org/10.1371/journal.pone.0110738] [PMID: 25356726]
[67]
Popinga A, Vaughan T, Stadler T, Drummond AJ. Inferring epidemiological dynamics with Bayesian coalescent inference: The merits of deterministic and stochastic models. Genetics 2015; 199(2): 595-607.
[http://dx.doi.org/10.1534/genetics.114.172791] [PMID: 25527289]
[68]
Cepeda JA, Odinokova VA, Heimer R, et al. Drug network characteristics and HIV risk among injection drug users in Russia: The roles of trust, size, and stability. AIDS Behav 2011; 15(5): 1003-10.
[http://dx.doi.org/10.1007/s10461-010-9816-7] [PMID: 20872063]
[69]
Gyarmathy VA, Li N, Tobin KE, et al. Injecting equipment sharing in Russian drug injecting dyads. AIDS Behav 2010; 14(1): 141-51.
[http://dx.doi.org/10.1007/s10461-008-9518-6] [PMID: 19214731]
[70]
Riabov GS, Kazennova EV, Korepanova LB, et al. The HIV-infection outbreak in the town Lys’va (Perm region): Homozygote genotype CCR5 delta32/CCR5 delta32 provides the high level of the persistence in the parenteral transmission of the virus. Vopr Virusol 2002; 47(4): 13-6.
[PMID: 12271718]
[71]
Heimer R, Barbour R, Shaboltas AV, Hoffman IF, Kozlov AP. Spatial distribution of HIV prevalence and incidence among injection drugs users in St Petersburg: Implications for HIV transmission. AIDS 2008; 22(1): 123-30.
[http://dx.doi.org/10.1097/QAD.0b013e3282f244ef] [PMID: 18090400]
[72]
Neshumaev DA. Screening of the population necessary to control the HIV epidemic. HIV Infect Immunosup Dis 2017; 9(3): 73-80.
[http://dx.doi.org/10.22328/2077-9828-2017-9-3-73-80]
[73]
Dmitrieva GM, Kostrykina TV, Metelev AA, et al. International scientific-practical conference actual problems of HIV. May 2016; People and health, St Petersburg, Russia 2016.
[74]
Pasechnik OA, Stasenko VL, Pischenco ND, et al. Prevalence of HIV infection among injecting drug users in the Siberian region Mod Prob Scie Edu 2017 [cited 2019 Feb 10] Available from: http://science-education.ru/ru/article/view?id=25907
[75]
Krasnoyarsk Drug Monitoring Report. [cited 2019 Feb 10]. Available from: http://www.krskstate.ru/safety/ank/info
[76]
Gashnikova NM, Safronov PF, Nikonorova YV, et al. Properties of CRF02_AG HIV-1 isolates circulating in Novosibirsk region. Zh Mikrobiol Epidemiol Immunobiol 2011; 3(3): 38-43.
[PMID: 21809643]